Echolocating toothed whales use ultra-fast echo-kinetic responses to track evasive prey
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Curated by eLife
Evaluation Summary:
This paper on echolocation-mediated responses to prey movements will be of interest to a broad audience, including ethologists and neuroscientists as well as those more generally interested in the natural world. Its strengths come from the use of data from both wild and captive animals of different species of toothed whales, as well as trained harbour porpoises, enabling generalization of the findings and conclusions on sensory-motor feedback.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Abstract
Visual predators rely on fast-acting optokinetic responses to track and capture agile prey. Most toothed whales, however, rely on echolocation for hunting and have converged on biosonar clicking rates reaching 500/s during prey pursuits. If echoes are processed on a click-by-click basis, as assumed, neural responses 100× faster than those in vision are required to keep pace with this information flow. Using high-resolution biologging of wild predator-prey interactions, we show that toothed whales adjust clicking rates to track prey movement within 50–200 ms of prey escape responses. Hypothesising that these stereotyped biosonar adjustments are elicited by sudden prey accelerations, we measured echo-kinetic responses from trained harbour porpoises to a moving target and found similar latencies. High biosonar sampling rates are, therefore, not supported by extreme speeds of neural processing and muscular responses. Instead, the neurokinetic response times in echolocation are similar to those of tracking responses in vision, suggesting a common neural underpinning.
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Author Response:
Reviewer #2 (Public Review):
[...] A potential weakness of this study could be that the tagged beaked whales were feeding in an uncontrolled setting. Relying on wild animals alone would limit the conclusions, as it is generally thought that predators use a feed-forward control system to anticipate prey movements and strike just as prey respond. Therefore, to bolster their investigation, the scientists conducted experimental trials on the trained porpoises in which the experimenters pulled on targets at varying speeds. [...] The very small sample size of this study, with just two animals of each species, could be seen as another limitation. However, it is difficult to work with live cetaceans, and this sort of sample size is not unusual for biologging research. Nonetheless, it would be helpful to know more about the …
Author Response:
Reviewer #2 (Public Review):
[...] A potential weakness of this study could be that the tagged beaked whales were feeding in an uncontrolled setting. Relying on wild animals alone would limit the conclusions, as it is generally thought that predators use a feed-forward control system to anticipate prey movements and strike just as prey respond. Therefore, to bolster their investigation, the scientists conducted experimental trials on the trained porpoises in which the experimenters pulled on targets at varying speeds. [...] The very small sample size of this study, with just two animals of each species, could be seen as another limitation. However, it is difficult to work with live cetaceans, and this sort of sample size is not unusual for biologging research. Nonetheless, it would be helpful to know more about the specimens. The data Vance et al. analyzed suggest that control bandwidths scale inversely with body length (e.g., with longer response latencies in larger animals). There was essentially no overlap in response times of the two porpoises, leaving one to wonder if one of the porpoises was notably larger. This sort of information would be useful to include in the paper. Also, potential extension of conclusions on response latencies to a range of other odontocetes, such as large sperm whales, would be useful. [...]
Thank you for your excellent summary of our manuscript in the public review. We are very gratified to see that the argument and key conclusions of the manuscript were transmitted clearly. The reviewer raises two limitations of the study. The first is due to the lack of control over predator motion during wild prey captures, in particular striking movements at prey. There is an inevitable trade-off between experimental control and ecological realism which we addressed in the study by contrasting data from 'natural experiments', involving wild animals, and controlled trials with trained animals. This also led us to focus on latency in click-rate adjustment as this may be more directly related to prey/target motion than is predator strike behaviour. We understand that the reviewer is satisfied with this solution.
The second limitation raised by the reviewer pertains to sample size. It is certainly difficult to collect high resolution biologging data from wild cetaceans, as the reviewer recognizes, leading to low sample sizes. However, the reviewer misstates the sample size of wild animals used in the manuscript: while we did work with only 2 captive harbour porpoise, in the wild studies we had a sample size of 6 harbour porpoise and 8 beaked whales (not two of each species as stated in the review).
The reviewer also asks if our conclusions could be extended to consider other odontocetes (e.g., sperm whales). This is an excellent point because the large distance between the brain and biosonar sound source in male sperm whales creates an additional source of latency. We have added mention of this to the revised manuscript.
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Evaluation Summary:
This paper on echolocation-mediated responses to prey movements will be of interest to a broad audience, including ethologists and neuroscientists as well as those more generally interested in the natural world. Its strengths come from the use of data from both wild and captive animals of different species of toothed whales, as well as trained harbour porpoises, enabling generalization of the findings and conclusions on sensory-motor feedback.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
The authors present a compelling investigation into the sensory-motor integration of echolocating toothed whales during prey capture. The strengths of this article reside on the use of data from both wild and captive animals of different species of toothed whales. This enables generalization of the findings and conclusions which strengthens the claims.
I have no major issues with this work. It is my opinion that a more thorough discussion on prey tracking behaviors and the evolutionary arms-race would situate the findings in a broader context and improve the manuscript.
I specifically liked the clever analyses presented in Figure 3 B-C for the wild animals. Though beyond the scope of this manuscript, it would be interesting to repeat the experiment with the captive animals tracking a target that moves …
Reviewer #1 (Public Review):
The authors present a compelling investigation into the sensory-motor integration of echolocating toothed whales during prey capture. The strengths of this article reside on the use of data from both wild and captive animals of different species of toothed whales. This enables generalization of the findings and conclusions which strengthens the claims.
I have no major issues with this work. It is my opinion that a more thorough discussion on prey tracking behaviors and the evolutionary arms-race would situate the findings in a broader context and improve the manuscript.
I specifically liked the clever analyses presented in Figure 3 B-C for the wild animals. Though beyond the scope of this manuscript, it would be interesting to repeat the experiment with the captive animals tracking a target that moves repeatedly (not isolated trials). In this same line, future studies including physiological methods (ABRs and EMGs to track muscle responses) could provide further insight into the processing times for the pathway proposed by the authors.
The manuscript is concise and clear. The methods are described appropriately. -
Reviewer #2 (Public Review):
To put their study in context, Vance and colleagues state (lines 83-84) that "the sensory feedback that echolocating predators receive from movements of their prey has received little attention." Although there has been considerable investigation of echolocation in odontocetes (toothed cetaceans) as well as in bats-which the authors point out together constitute a remarkable one fourth of all mammals-there have been no successful attempts to compare the kinematic and neural tracking responses of echolocating predators with that of visual predators (such as in well-studied primates).
The echolocation system of both odontocetes and bats works exactly like sonar: high frequency sonic pulses are emitted, and their reflections are detected to provide information about their surrounding environment, such as …
Reviewer #2 (Public Review):
To put their study in context, Vance and colleagues state (lines 83-84) that "the sensory feedback that echolocating predators receive from movements of their prey has received little attention." Although there has been considerable investigation of echolocation in odontocetes (toothed cetaceans) as well as in bats-which the authors point out together constitute a remarkable one fourth of all mammals-there have been no successful attempts to compare the kinematic and neural tracking responses of echolocating predators with that of visual predators (such as in well-studied primates).
The echolocation system of both odontocetes and bats works exactly like sonar: high frequency sonic pulses are emitted, and their reflections are detected to provide information about their surrounding environment, such as obstacles to be avoided or food items to be gained. It has long been recognized that when odontocetes and bats approach targeted prey, their distinct clicks are produced increasingly rapidly, producing, in one burst, what sounds to people like a single buzz.
The so-called "interclick interval" [ICI] between the individual clicks within this buzz are extraordinarily brief-about 2 to 4 milliseconds. It has been assumed, but never really addressed previously, that odontocetes process this information quickly and make use of all the incredibly rapid clicks to adjust their approach to prey. However, this idea has not been properly studied via scientific investigation. Could it be that the brief IC intervals simply relate to how the clicks are produced, due to the anatomy of the nasal passages or the physiology of the odontocete sound production system? In other words, do these rapid clicks translate to rapid brain processing? This is an important question because primates and other visual predators also use rapid signal processing, but at a rate 10-20 times slower than the odontocete buzzes-about 50 to 200 milliseconds. This neural processing of visual predators (roughly a tenth of a second on average) has been described as "ultrafast." Could odontocete brains work even faster?
Vance and colleagues collected data from digital logging tags affixed to the backs of two odontocete species: beaked whales that live in the deep open ocean, as well as trained captive porpoises that live in shallow coastal waters. The combination of two species (and habitats), and the inclusion of controlled study from the captive porpoises, is a real strength of this study. A potential weakness of this study could be that the tagged beaked whales were feeding in an uncontrolled setting. Relying on wild animals alone would limit the conclusions, as it is generally thought that predators use a feed-forward control system to anticipate prey movements and strike just as prey respond. Therefore, to bolster their investigation, the scientists conducted experimental trials on the trained porpoises in which the experimenters pulled on targets at varying speeds. This enabled the researchers to confirm that even sudden, unpredictable movements of evasive prey do not affect the results. The porpoises could respond to rapid movements of their intended targets, but the response latencies were not instant and did not correspond to individual clicks; instead, they spanned many clicks.
The study’s small sample size, particularly of captive animals, with just two captive harbor porpoises along with six wild harbor porpoises and eight beaked whales, could be seen as another limitation. However, it is difficult to work with live cetaceans, and this sort of sample size is not unusual for biologging research. Nonetheless, it would be helpful to know more about the specimens. The data Vance et al. analyzed suggest that control bandwidths scale inversely with body length (e.g., with longer response latencies in larger animals). There was essentially no overlap in response times of the two porpoises, leaving one to wonder if one of the porpoises was notably larger. This sort of information would be useful to include in the paper. Also, potential extension of conclusions on response latencies to a range of other odontocetes, such as large sperm whales, would be useful.
Nonetheless, the combined data strongly support the conclusion that odontocetes process sound signals about as fast as visual predators-in other words, much more slowly than the abundant acoustic signals arrive. This finding-that there is a confirmed mismatch between odontocetes' sound production (during close-approach buzzes) and their motor control-is important. The combination of similar data from wild beaked whales and captive porpoises in a controlled setting serves to strengthen the conclusions. Not only are these diverse, distantly related odontocetes both relying on the same mechanism, but they are also responding at roughly the same speed as predators that track prey visually. It is not hard to agree with the conclusion that mammals' biosonar response is akin to the visual response.
Thus the researchers conclude that there is likely an "echokinetic" response similar to the well-studied "optokinetic response" of mammals. Perhaps this stems from common evolution of mammalian brains and neurophysiology before these types of predators diverged and evolved different habitats and prey capture methods, or perhaps it is due to simple limitations of neural processing. Either way, the authors present a solid case that "echo processing and control decisions during buzzes are decoupled from click rate" (line 270), which means that echolocation does not require extremely fast brain speeds.
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